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Colonization Kinetics and Implantation Follow-Up of the Sewage Microbiome in an Urban Wastewater Treatment Plant

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Colonization Kinetics and Implantation Follow-Up of the Sewage Microbiome in an Urban Wastewater Treatment Plant www.nature.com/scientificreports OPEN Colonization kinetics and implantation follow‑up of the sewage microbiome in an urban wastewater treatment plant Loïc Morin1, Anne Goubet2, Céline Madigou2, Jean‑Jacques Pernelle2, Karima Palmier1, Karine Labadie3, Arnaud Lemainque3, Ophélie Michot4, Lucie Astoul4, Paul Barbier5, Jean‑Luc Almayrac4 & Abdelghani Sghir5* The Seine-Morée wastewater treatment plant (SM_WWTP), with a capacity of 100,000 population- equivalents, was fed with raw domestic wastewater during all of its start‑up phase. Its microbiome resulted from the spontaneous evolution of wastewater‑borne microorganisms. This rare opportunity allowed us to analyze the sequential microbiota colonization and implantation follow up during the start-up phase of this WWTP by means of regular sampling carried out over 8 months until the establishment of a stable and functional ecosystem. During the study, biological nitrifcation– denitrifcation and dephosphatation occurred 68 days after the start-up of the WWTP, followed by focs decantation 91 days later. High throughput sequencing of 18S and 16S rRNA genes was performed using Illumina’s MiSeq and PGM Ion Torrent platforms respectively, generating 584,647 16S and 521,031 18S high-quality sequence rDNA reads. Analyses of 16S and 18S rDNA datasets show three colonization phases occurring concomitantly with nitrifcation, dephosphatation and foc development processes. Thus, we could defne three microbiota profles that sequentially colonized the SM_WWTP: the early colonizers, the late colonizers and the continuous spectrum population. Shannon and inverse Simpson diversity indices indicate that the highest microbiota diversity was reached at days 133 and 82 for prokaryotes and eukaryotes respectively; after that, the structure and complexity of the wastewater microbiome reached its functional stability. This study demonstrates that physicochemical parameters and microbial metabolic interactions are the main forces shaping microbial community structure, gradually building up and maintaining a functionally stable microbial ecosystem. Te wastewater treatment process is based on the use of sludge microbial populations to treat domestic and indus- trial pollutants. Tese populations constitute a complex ecosystem with biomass concentration approximating 2–10 g L−11, with the majority aggregated into structures called focs. Te foc structure represents a protection strategy for microorganisms against predation as well as toxic chemicals, meanwhile allowing efcient uptake of nutrients. Tese focs may contain up to 1010 prokaryotes mL−1 and 106 micro-eukaryotes mL−1. Molecular approaches reveal that they ofen share persistent prokaryotic and eukaryotic core species stably retained over time, including among others, members of the Proteobacteria, Bacteroidetes, Firmicutes, and Actinobacteria phyla2–4. However, in comparison with prokaryotes, micro-eukaryotic diversity has benefted relatively little from modern molecular tools and high throughput sequencing technologies. Te few sequencing-based analyses 1Institut de Biologie Intégrative de la Cellule, Université Paris Saclay, 91405 Orsay Cedex, France. 2INRAE, PROSE, Université Paris-Saclay, 92761 Antony, France. 3Genoscope, Institut de Biologie François-Jacob, CEA, Université Paris-Saclay, 91057 Evry, France. 4Laboratoire SIAAP Site Seine Amont, Usine Marne Aval, 100 rue de la Plaine, 93160 Noisy-Le-Grand, France. 5Génomique métabolique, Genoscope, Institut de Biologie François Jacob, CEA, CNRS, Université d’Evry, Université Paris-Saclay, 91057 Evry, France. *email: [email protected] SCIENTIFIC REPORTS | (2020) 10:11634 | https://doi.org/10.1038/s41598-020-68496-z 1 Vol.:(0123456789) www.nature.com/scientificreports/ performed on samples from WWTP or sewage treatment bioreactors suggest that large knowledge gaps in diversity and functional ecology of this group of microorganisms 5–8 exist, preventing accurate defnitions of their identity, diversity and their roles in the depollution process. To provide a holistic view of the functioning of whole ecosystems, major fundamental studies are necessary for assessing the network of interactions between all kinds of microbes (Bacteria, Archaea, Eukarya and viruses) and with their environment. Tis will permit the inference of the ecological rules guiding assembly of complex microbial communities and their functional impli- cations across temporal gradients, and biological and physicochemical perturbations, which still await discovery. Such studies should help anticipate the structure and activity of microbial communities and consequently the functional stability of the ecosystem. Recent studies have reported temporal variations in both composition and structure of microbial communities9,10. To the best of our knowledge, no work has studied the colonization kinetics and the estab- lishment of the wastewater microbiome through to the constitution of a complex and functional microbial ecosystem. In the present study, we are taking advantage of the start-up of a domestic WWTP to achieve full characterization of 23 time series samples from the SM_WWTP over 236 days. We hence, followed the coloni- zation kinetics of wastewater-borne microorganisms from March 3rd through October 31st, 2014, using high throughput prokaryotic 16S and eukaryotic 18S rRNA gene sequencing, until the establishment of a complex functional and stable ecosystem. Results Physicochemical and overall molecular diversity analyses of microbial populations. Te infor- mation regarding plant localization and process description, variation of plant operational parameters and phys- icochemical conditions, treatment performance, are detailed in Supplementary material online (Fig. S1, Fig. S2 and Table S1). Nitrogen measurement defnes three periods: (1) Te frst period lasts for 11 weeks (13–40 days) during which ammonia in the aerobic basin is at its maximal concentration. (2) In the second period that lasts about 1 month, the ammonia starts decreasing concomitantly with the appearance of nitrite (day 40) and nitrate (day 68), until day 133 (Fig. 1A). (3) In the third period (133–236 days) nitrite is completely oxidized to nitrate at day 133 and remains relatively stable during the rest of the time. Biological dephosphatation started at day 40, and phosphorus concentration fuctuated from day 68 through day 133, to be completely reduced over this third period (133–236 days). Flocs decantation appeared 91 days afer the start-up of the SM_WWTP. Principal component analyses of the microbiota 16S and 18S rDNA data sets, revealed a diversifcation in microbial composition between samples, concomitantly occurring with the physicochemical transformations (e.g. nitrifcation, dephosphatation and foc development processes). Tis analysis indicates the constitution of three main homogeneous prokaryotic groups (Fig. 1B) whereas 18S rDNA tags indicates four eukaryotic groups (Fig. 1C). Afer stabilization, the plant could efectively remove 97.8% of chemical oxygen demand (COD) and 99.6% biological oxygen demand (BOD) from the sewage (Table S1). A total of 584,647 and 521,031 high quality reads were generated from 23 SM_WWTP rDNA amplicon sequencing (Table 1), with an average of 25,419 and 22,653 reads per sample for bacteria and eukaryotes respec- tively. Phylotype richness calculation for individual samples based on the construction of rarefaction curves shows a complete saturation of microbial diversity (Fig. S3A, Fig. S3B). Sequence read clustering, based on 97% sequence similarity reveals, the occurrence of 6,696 bacterial operational taxonomic units (OTUs) and 1,423 eukaryotic OTUs (Table 1). Taxonomic afliations using Silva database-132 shows that the 6,696 bacterial OTUs afliated with 36 phyla among which we describe 30 persistent OTUs, occur at various abundancies through- out the study (Table 1). Among the 1,423 eukaryotic OTUs, we describe 19 persistent OTUs afliating with 15 phyla (Table 1). Shannon and Inverse Simpson diversity indices show the occurrence of two periods, the frst one where microbiota increase in numbers and diversity and the second period where the microbiota reaches its steady state (Fig. 1F,G). Overall description of wastewater microbiota phylogenetic groups. Te most predominant phy- logenetic groups within the Bacteria domain are the Gram-negative bacteria, represented by Proteobacteria and Bacteroidetes, and the Gram-positives represented by Firmicutes and Actinobacteria, averaging 64.8% and 13.1% of the total number of OTUs respectively. Planctomycetes, Chlorofexi, Verrucomicrobia, and Acidobacteria, rep- resent an average of 17.6% of the total OTUs. Te remaining 28 minor phylogenetic groups account for only 4.5%. In terms of abundance, nine phylogenetic groups, Proteobacteria, Bacteroidetes, Planctomycetes, Chloro- fexi, Firmicutes, Actinobacteria, Acidobacteria, Gemmatimonadetes, and Patescibacteria (Saccharibacteria) rep- resent up to 97.6% of the total reads (Fig. S5A), whereas the remaining 27 minor phyla made up only 2.4% of the total reads. Inside these phyla, the distribution of subphyla follows the same pattern, with major and minor sub- phyla (Fig. S5A). On the other hand, the distribution of genera abundance is characterized by a large diversity, i.e. many genera with a low abundance. However, some genera emerge with a slightly more elevated abundance; such is the case for Acinetobacter, an unknown genus from Gammaproteobacteria, Terrimonas, and an unknown genus from Saprospiraceae, and Flavobacterium, that together
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